Synopsis
Typical and Atypical
Enteropathogenic Escherichia coli
Luiz R. Trabulsi,* Rogéria Keller,* and Tânia A. Tardelli Gomes†
*Laboratório Especial de Microbiologia, Instituto Butantan,
São Paulo, Brazil; and †Universidade Federal de São Paulo, São Paulo,
Brazil
Typical and
atypical enteropathogenic Escherichia coli (EPEC) strains
differ in several characteristics. Typical EPEC, a leading cause
of infantile diarrhea in developing countries, is rare in industrialized
countries, where atypical EPEC seems to be a more important cause
of diarrhea. For typical EPEC, the only reservoir is humans; for
atypical EPEC, both animals and humans can be reservoirs. Typical
and atypical EPEC also differ in genetic characteristics, serotypes,
and virulence properties. Atypical EPEC is more closely related
to Shiga toxin–producing E. coli (STEC), and like STEC
these strains appear to be emerging pathogens.
Enteropathogenic Escherichia coli (EPEC) is a leading cause
of infantile diarrhea in developing countries. In industrialized
countries, the frequency of these organisms has decreased, but they
continue to be an important cause of diarrhea (1).
The central mechanism of EPEC pathogenesis is a lesion called attaching
and effacing (A/E), which is characterized by microvilli destruction,
intimate adherence of bacteria to the intestinal epithelium, pedestal
formation, and aggregation of polarized actin and other elements
of the cytoskeleton at sites of bacterial attachment (Figure
1). The fluorescent actin staining test allows the identification
of strains that produce A/E lesions, through detection of aggregated
actin filaments beneath the attached bacteria (3).
Ability to produce A/E lesions has also been detected in strains
of Shiga toxin–producing E. coli (enterohemorrhagic E.
coli [EHEC]) and in strains of other bacterial species (1).
|
Figure
1 |
|
|
|
|
|
Click
to view enlarged image
Figure 1. Attaching and
effacing lesion showing effacement of microvilli (mv) and
pedestal (star) with adherent enteropathogenic Escherichia
coli (EPEC) (arrow)....
|
|
|
|
|
|
Figure
2
|
|
|
|
|
|
Click
to view enlarged image
Figure 2. Diagram of the
main genes of the locus of enterocyte effacement (LEE) region
and the enteropathogenic Escherichia coli (EPEC) adherence
factor (EAF) plasmid. |
|
The genetic determinants for the production of A/E lesions are
located on the locus of enterocyte effacement (LEE) (4),
a pathogenicity island that contains the genes encoding intimin,
a type III secretion system, a number of secreted (Esp) proteins,
and the translocated intimin receptor named Tir (1)
(Figure 2). Two LEE insertion sites have
been described on the E. coli chromosome, and a third unidentified
insertion site has been reported (5).
Intimin, a 94-kDa outer membrane protein encoded by the eae
gene, is responsible for the intimate adherence between bacteria
and enterocyte membranes. Studies of antigenic variations in the
280-amino acid residues of the C-terminal portion of intimin (the
receptor-binding domain of the protein) and the use of polymerase
chain reaction analysis allow the classification of distinct intimin
types or subtypes among EPEC and STEC strains (6).
The Esp molecules (EspA, B, and D) are involved in the formation
of a translocon that delivers effector molecules to the host cell
and disrupts the cytoskeleton, subverting the host cell functions
(7). Tir, which is one of the EPEC translocated
proteins, is inserted into the host cell membrane, where it acts
as a receptor to intimin (8).
Many EPEC strains produce a characteristic adherence pattern, called
localized adherence, in tissue culture cells (9).
In this pattern, bacteria bind to localized areas of the cell surface,
forming compact microcolonies (bacterial clusters) that can be visualized
after bacteria have been in contact with cells for 3 hours. This
phenomenon is associated with the presence of the large EPEC adherence
factor (EAF) plasmid, which carries the so-called EAF sequence (Figure
2) (1). Also present in the EAF plasmid is
the cluster of genes that encode bundle-forming pili (BFP), which
interconnect bacteria within microcolonies and thus promote their
stabilization (1).
The EAF plasmid is not essential for the formation of A/E lesions,
although its presence enhances their efficiency, probably through
the influence of a cluster of plasmid-borne regulatory genes (per
A, B, C) that increase expression of the chromosomal
LEE genes (1). Evidence also indicates that BFP
plays a role in host cell adhesion that would similarly increase
the efficiency of A/E lesion formation (7).
In 1995, during the Second International Symposium on EPEC in São
Paulo, most participants accepted the following EPEC definition:
“EPEC are diarrheogenic Escherichia coli that produce a characteristic
histopathology known as attaching and effacing (A/E) on intestinal
cells and that do not produce Shiga, Shiga-like, or verocytotoxins.
Typical EPEC of human origin possess a virulence plasmid known as
the EAF (EPEC adherence factor) plasmid that encodes localized adherence
on cultured epithelial cells mediated by the . . . Bundle Forming
Pilus, while atypical EPEC do not posses this plasmid. The majority
of typical EPEC strains fall into certain well-recognized O:H serotypes”
(10). According to this definition, the basic difference
between typical and atypical EPEC is the presence of the EAF plasmid
in the first group of organisms and its absence in the second.
The most studied EPEC strains belong to a series of O antigenic
groups known as EPEC O serogroups. Twelve EPEC serogroups were recognized
by the World Health Organization in 1987: O26, O55, O86, O111, O114,
O119, O125, O126, O127, O128, O142, and O158. These serogroups include
both typical and atypical EPEC strains, as well as other diarrheogenic
E. coli categories, mainly enteroaggregative E. coli
(EAEC) (11-14). Furthermore, most of the strains
of each category correspond to specific serotypes in each O serogroup.
The division of EPEC strains into typical and atypical has important
implications that are not yet fully appreciated. EPEC can no longer
be considered as a single group of enteropathogenic organisms. The
aim of this article is to review the main differences between typical
and atypical EPEC, which should be taken into account in studies
involving these organisms.
Serotypes
Typical and atypical EPEC strains belong to two different sets
of serotypes (Table 1). This table was constructed
on the basis of similar studies carried out in São Paulo (11-15)
and the United Kingdom (14) and on a smaller scale
in Rio de Janeiro (16) and Italy (17).
Most of the typical strains were isolated in São Paulo and Rio de
Janeiro and most of the atypical ones in United Kingdom and in Italy.
The serotypes isolated in São Paulo include motile and nonmotile
strains (indicated by placing the H antigen in brackets). The H
antigens of these nonmotile strains were inferred by restriction
analysis of the fliC genes (B.A. Botelho, et al., unpub.
data). These serotypes may include both motile and nonmotile variants
(Table 1).
Most of the serotypes in Table 1 may easily
be classified as typical or atypical. However, some serotypes are
not so readily classified, mainly those that include Stx-producing
strains, of which the most frequent are serotypes O26:H- and H11,
and O111ac:[H8](considered by some authors as EHEC or STEC) (1).
In fact, these serotypes and others with properties similar to those
of O128:H2 are not true atypical EPEC or STEC serotypes but rather
are heterogeneous serotypes that include different clones or genetic
lineages. For example, we have recently shown by random amplified
polymorphic DNA that O26:H11 Stx-producing strains isolated in Europe
and North America are genetically different from Stx-negative strains
of the same serotype isolated in Brazil (18).
Although this kind of study has not been done with serotype O128:H2,
this serotype is also heterogeneous since it includes different
ribotypes with distinct virulence characteristics (L.R. Trabulsi
et al., unpub. data). Certain Stx-producing clones have an irregular
geographic distribution and so may be found in some countries but
not in others. Other characteristics that may complicate distinguishing
typical from atypical EPEC are related to the EAF plasmid markers.
For example, serotypes O119:H2 and O128:H2 react with the bfpA
probe but do not have a true EAF plasmid. These serotypes have a
100-MDa plasmid that does not contain the bfp operon and
consequently does not produce BFP (19). In contrast,
some O142:H6 strains do not react with the EAF probe but produce
BFP and show a typical localized adherence (LA) pattern. These strains
may have an EAF plasmid with a defect in the EAF region that does
not interfere with the the plasmid’s functions. Perhaps the best
distinguishing characteristic for typical and atypical EPEC serotypes
would be production or nonproduction of BFP.
Virulence
Characteristics
In general, typical EPEC strains are more homogeneous in their
virulence characteristics than the atypical ones. With few exceptions,
typical strains produce only the virulence factors encoded by the
LEE region and the EAF plasmid. The exceptions are the production
of the cytolethal distending toxin (CDT) by all O86:H34 strains
(L.R. Trabulsi et al., unpub. data) and the production of
the enteroaggregative heat stable toxin (EAST1) by some strains
of serotypes O55:H6 and O127:H6 (T.A.T.Gomez et al., unpub. data)
that are potential virulence factors. In contrast, atypical EPEC
strains frequently express EAST1 and other potential virulence factors
not encoded in the LEE region (Table 2). Accordingly,
there are two kinds of atypical EPEC strains: those that express
only the LEE-encoded virulence factors and those that express both
LEE and the non-LEE encoded virulence factors. Usually both kinds
of strains belong to a single clone (11,12,15).
All atypical EPEC serotypes, with exception of O125ac:H6, include
both kinds of strains. All strains of this serotype examined thus
far show the aggregative adherence pattern and the LEE region. The
occurrence of more than one kind of strain in most atypical serotypes
is another interesting difference between typical and atypical EPEC.
|
Figure
3 |
|
|
|
|
|
Click
to view enlarged image
Figure 3. Adherence patterns
of enteropathogenic Escherichia coli (EPEC) strains.
Localized adherence (LA), diffuse adherence (DA), aggregative
adherence (AA), and localized adherence-like (LAL). Magnification:
X100.
|
|
|
|
|
|
Figure
4
|
|
|
|
|
|
Click
to view enlarged image
Figure 4. Dendogram
to illustrate genetic differences between typical and atypical
enteropathogenic Escherichia coli (EPEC) strains and
E. coli O157:H7 strains. |
|
Typical and atypical EPEC strains also differ in adherence patterns.
The typical strains show only the LA pattern, while atypical strains
may show the LAL (localized-like adherence) pattern (12),
the DA (diffuse adherence) pattern, or the AA (aggregative adherence)
pattern (Figure 3). The LAL pattern is characteristic
of the strains of most serotypes and is mediated mainly by intimin
(20). The DA pattern is mediated by the Afa adhesin
(R. Keller et al., unpub. data), and the AA is mediated by an aggregative
adhesin. The cdt gene of serotype O86:H34 (L.R. Trabulsi
et al., unpub. data) and the afa gene of serotype O55:H7
are located on the bacterial chromosome (R. Keller et al., unpub.
data). Typical and atypical EPEC also have some interesting differences
with regard to the intimin types (Table 3).
Genetic
Relationships
To investigate the genetic relationships between typical and atypical
EPEC strains, we used random amplified polymorphic DNA to study
our collection of strains, which includes most of the serotypes
shown in Table 1. The dendrogram derived from
these data (Figure 4) shows that most typical
and atypical strains belong to different genetic groups and that
the atypical strains are closer to the serotype O157:H7 strains
(EHEC), which were included in the study for comparison purposes
(S.Y.Bando et al., unpub. data). The only exceptions were the typical
and atypical H2 strains that did not separate and formed a subgroup
in the atypical/STEC group. The overall results of this study resemble
those reported by Whittam et al. (21), who used
multilocus enzyme electrophoresis to study a similar collection
of strains and distinguished four genetic groups: EPEC 1 (H6/H34
strains), EPEC 2 (H2 strains), EHEC 1 (O55:H7 and O157:H7 strains),
and EHEC 2 (O26:H11 and O111ac:H- strains). The EPEC 2 group was
also closer to the EHEC groups. For this article, we have not used
the division of EPEC into EPEC 1 and EPEC 2, but it may be important
in the future. Several other differences exist between the two clonal
groups (R. Keller et al., unpub. data). With regard to epidemiology,
an EPEC 2 serotype (O111:H2) is strongly associated with nosocomial
infection, while an EPEC 1 serotype (O119:H6) is more strongly associated
with infection in the community (22).
Pathogenicity
The pathogenicity of most typical EPEC serotypes has been confirmed
by volunteer studies (1). For atypical EPEC we
are aware of only one volunteer study, which was performed by Levine
et al. (23) with an O128:H2 strain. This strain
was administered in differing doses to 15 adult volunteers, none
of whom became ill. Although this study was carefully conducted,
its results are difficult to evaluate because the virulence characteristics
of the strain were not known and serotype O128:H2 may include nonvirulent
strains (24).
The atypical EPEC strains may be less virulent than the typical
ones. One reason may be the lack of the EAF plasmid; Levine et al.
(25) have shown that an O127:H6 strain without
plasmid was less virulent for adult volunteers than the wild-type
strain. However, atypical EPEC strains have not been proven to be
less pathogenic, and these organisms have other virulence factors
that may compensate for the absence of the EAF plasmid. More studies
are necessary to resolve this issue.
Association
with Diarrhea
Typical EPEC serotypes are strongly associated with diarrhea in
children <1 year of age. In this age group, these serotypes have
been found to be the main cause of endemic diarrhea in several well-controlled
studies carried out in Brazil (26,27). The frequency
of typical EPEC serotypes in children >1 year of age is lower
and similar to the frequency in controls (2%-4%). Adult infections
are rare and usually associated with other conditions (1).
The increased resistance in older children and adults may be associated
with the development of immunity or the loss of receptors for some
specific adhesin (1).
Regarding immunity, several studies carried out in Brazil (28)
and more recently in Mexico (29) have shown that
children develop high levels of antibody against the main EPEC virulence
factors. In addition, the colostrum of mothers living in endemic
areas is very rich in immunoglobulin A antibodies against the EPEC
virulence factors (28-30). Much less is known
about the association of atypical serotypes with diarrhea, but usually
these serotypes are isolated from children with diarrhea who are
not carriers of other enteropathogenic agents. A strong association
of atypical EPEC serotypes with endemic diarrhea has not yet been
demonstrated. However, a large outbreak of diarrhea caused by serotype
O111:H9 has been described in Finland (31).
Prevalence
in Developing and Industrialized Countries
A remarkable epidemiologic difference between typical and atypical
EPEC serotypes is their geographic distribution. Typical EPEC serotypes
have traditionally been associated with outbreaks of infantile diarrhea,
and, in fact, the first EPEC strains isolated in different countries
were of serotypes O55:H6 and O111:H2 (32). In
the past, these epidemic serotypes were frequently identified in
industrialized countries as a cause of outbreaks and sporadic cases
of diarrhea, but at present they are very rare (1).
In these countries today, serotypes without the EAF plasmid predominate
(14,33). In the United Kingdom,
for example, EAF-positive strains represent only 10% of all EPEC
strains (14). The situation in developing countries
is not well defined, but several studies in Brazil in the 1980s
and early 1990s showed a high frequency of typical serotypes (34).
However, some recent studies have shown a very low frequency of
typical EPEC and a relatively high frequency of atypical EPEC (L.C.
Campos, pers. commun. and unpub. data). This finding coincides with
a decline in the number of diarrheal cases in several regions in
Brazil, suggesting that the changes that have occurred in industrialized
countries are likely already under way in Brazil. The reason for
these changes is not clear, but the decline in the frequency of
the EAF-positive serotypes that has occurred in Europe and the United
States and is beginning to occur in Brazil may be due to improvements
in therapy, sanitary conditions, and control of hospital infections.
On the other hand, the emergence and rise in frequency of atypical
EPEC strains may have origins similar to those that led to the emergence
and increase in frequency of O157:H7 and other STEC serotypes (35).
Reservoir
Typical EPEC serotypes have not been found in animals (1),
suggesting that humans are the only living reservoir for these organisms.
In contrast, most atypical EPEC serotypes have been isolated from
different animal species. The association between serotype O26:H11
and calves is well known (36). Recent studies
have emphasized the isolation of Stx-producing strains because of
their role in hemolytic uremic syndrome, but eae-positive,
Stx-negative strains have been isolated from cattle (37).
This kind of strain should be considered atypical EPEC. A similar
situation exists in regard to serotype O111ac, and the 69 O111ac
strains reported by Ewing et al. in 1963 were all isolated from
monkeys (38).
Serotype O128:H2 is rather frequent in rabbits and dogs and, like
the human strains isolated in Brazil, is EAF negative (Pestana de
Castro, pers. commun.). In a recent study by Pestana de Castro’s
group, serotypes O119:H2 and O111:H25 (an EAF-negative serotype
rare in Brazil but frequent in the United Kingdom) were isolated
frequently from dogs. More studies of the prevalence of atypical
EPEC serotypes in animals are needed, but available data strongly
suggest that the primary reservoir for these organisms is different
animal species, as is the case with STEC strains.
Stx-Negative
and eae-Positive E. coli Strains in Non-EPEC O Serogroups
Both stx-negative and eae-positive E. coli strains
are found in many non-EPEC O serogroups (39).
We have detected such strains in more than 30 E. coli O serogroups,
and a large proportion of strains do not agglutinate in the usual
set of E. coli O antisera. Some strains react with the EAF
probe (eae+, EAF+ strains), but most do not react with this
probe (eae+, EAF- strains). With a few exceptions, only one
or two strains of each of these serotypes have been reported (40).
The additional virulence characteristics of the eae+, EAF+
strains have not been studied, but recently we investigated the
virulence profile of 49 different eae+, EAF- strains isolated
from children with diarrhea in São Paulo. The profile was similar
to that of atypical EPEC: many strains were EAST1+ and E-hly+,
and a few expressed either the AA or the DA adherence pattern. Some
strains had the gamma intimin sequence, and in many of the strains
the intimin type could not be identified.
Some of these strains do correspond to typical or atypical EPEC,
and more studies are necessary to establish a precise concept for
them, especially for the EAF-negative strains. Some are likely STEC
strains that have lost the stx genes; we cannot exclude the
possibility that the DA and AA strains are not true EAEC or DAEC
that have received the LEE pathogenicity island by horizontal transfer.
The situation is quite different for atypical EPEC, since a larger
number of strains have been studied and most of them belong to well-characterized
serotypes.
The role played by these EAF+ and EAF- strains outside the EPEC
serogroups in endemic diarrhea has not been established. In general,
the strains are rarely isolated from diarrheal cases and controls,
and the global difference is not statically significant. However,
some eae+, EAF+ serotypes as well as some eae+, EAF-
strains with specific virulence profiles seem to be associated with
endemic diarrhea (2,33,40). With
regard to outbreaks, an eae+, EAF- serotype (O39:H-) was
responsible for a foodborne diarrheal outbreak in 1991, involving
100 adults in Minnesota (41).
Conclusion
Typical and atypical EPEC seem to constitute two groups of distinct
organisms that have in common the LEE pathogenicity island. Atypical
EPEC are closer to STEC in genetic characteristics, serotypes, production
of toxins, reservoir, and other epidemiologic aspects. As STEC,
they resemble emerging pathogens. In industrialized countries, they
have become a more frequent cause of diarrhea than typical EPEC,
and the same shift may be occurring in Brazil. A large number of
Stx-negative, eae-positive typical and atypical EPEC-like
strains outside the EPEC O serogroups, as well as atypical EPEC
strains, require further study in regard to their virulence and
epidemiologic significance.
Acknowledgments
We thank James Kaper for reviewing this article and Gad Frankel
for useful discussion.
These studies were supported by FINEP/MCT/PRONEX grant (41.96.0881.00),
PADCT/CNPq grant (62.0236/92-2), and FAPESP grants (92/04890-2 and
00/05256-3) awarded to L.R.T., as well as FAPESP grant (95/9176-4)
to T.A.T.G.
Dr. Trabulsi is emeritus professor of the University of São Paulo
and director of Laboratório Especial de Microbiologia do Instituto
Butantan, São Paulo.
References
- Nataro JP, Kaper JB.
Diarrheogenic Escherichia coli. Clin Microbiol Rev
1998;11:142-201.
- Pedroso MZ, Freymuller E, Trabulsi LR, Gomes TA. Attaching-effacing
lesions and intracellular penetration in HeLa cells and human
duodenal mucosa by two Escherichia coli strains not belonging
to the classical enteropathogenic E. coli serogroups.
Infect Immun 1993;61:1152-6.
- Knutton S, Baldwin T, Williams PH, McNeish AS.
Actin accumulation at sites of bacterial adhesion to tissue culture
cells: basis of a new diagnostic test for enteropathogenic and
enterohemorrhagic Escherichia coli. Infect Immun 1989;57:1290-8.
- McDaniel TK, Jarvis KG, Donnenberg MS, Kaper JB. A
genetic locus of enterocyte effacement conserved among diverse
enterobacterial pathogens. Proc Natl Acad Sci U S A 1995;92:1664-8.
- Sperandio V, Kaper JB, Bortolini MR, Neves BC, Keller R, Trabulsi
LR. Characterization
of the locus of enterocyte effacement (LEE) in different enteropathogenic
Escherichia coli (EPEC) and Shiga-toxin producing Escherichia
coli (STEC) serotypes. FEMS Microbiol Lett 1998;164:133-9.
- Adu-Bobie J, Frankel G, Bain C, Goncalves AG, Trabulsi LR, Douce
G, et al. Detection
of intimins alpha, beta, gamma, and delta, four intimin derivatives
expressed by attaching and effacing microbial pathogens. J
Clin Microbiol 1998;36:662-8.
- Frankel G, Phillips AD, Rosenshine I, Dougan G, Kaper JB, Knutton
S. Enteropathogenic
and enterohaemorrhagic Escherichia coli: more subversive
elements. Mol Microbiol 1998;30:911-21.
- Kenny B, Devinney R, Stein M, Reinscheid DJ, Frey EA, Finlay
BB. Enteropathogenic
Escherichia coli (EPEC) transfers its receptor for intimate
adherence into mammalian cells. Cell 1997;91:511-20.
- Scaletsky ICA, Silva MLM, Trabulsi LR. Distinctive
patterns of adherence of enteropathogenic Escherichia coli
to HeLa cells. Infect Immun 1984;45:534-6.
- Kaper JB. Defining EPEC. Rev Microbiol 1996;27:130-3.
- Campos LC, Whittam TS, Gomes TAT, Andrade JRC,
Trabulsi LR. Escherichia
coli
serogroup O111 includes several clones of diarrheogenic strains
with diferrent virulence properties. Infect Immun 1994;62:3282-8.
- Rodrigues J, Scaletsky ICA, Campos LC, Gomes TAT, Whittan ST,
Trabulsi LR.
Clonal structure and virulence factors in strains of Escherichia
coli of the classic serogroup O55. Infect Immun 1996;64:2680-6.
- do Valle GR, Gomes TA, Irino K, Trabulsi LR. The
traditional enteropathogenic Escherichia coli (EPEC) serogroup
O125 comprises serotypes which are mainly associated with the
category of enteroaggregative E. coli. FEMS Microbiol
Lett 1997;152:95-100.
- Scotland SM, Smith HR, Cheasty T, Said B, Willshaw GA, Stokes
N, et al. Use
of gene probes and adhesion tests to characterize Escherichia
coli belonging to enteropathogenic serogroups isolated in
the United Kingdom. J Med Microbiol 1996;44:438-43.
- Gonçalves AG, Campos LC, Gomes TA, Rodrigues J, Sperandio V,
Whittam TS, et al. Virulence
properties and clonal structures of strains of Escherichia
coli O119 serotypes. Infect Immun 1997;65:2034-40.
- Rosa AC, Mariano AT, Pereira AM, Tibana A, Gomes TAT, Andrade
JR. Enteropathogenicity
markers in Escherichia coli isolated from infants with
acute diarrhoea and healthy controls in Rio de Janeiro, Brazil.
J Med Microbiol 1998;47:781-90.
- Giammanco A, Maggio M, Giammanco G, Morelli R, Minelli F, Scheutz
F, et al.
Characteristics of Escherichia coli strains belonging to
enteropathogenic E. coli serogroups isolated in Italy from
children with diarrhea. J Clin Microbiol 1996;34:689-94.
- Peixoto J, Bando S, Ordoñez J, Botelho B, Trabulsi L, Moreira-Filho
C. Genetic
differences between Escherichia coli O26 strains isolated
in Brazil and in other countries. FEMS Microbiol Lett 2001;196:239-44.
- Bortolini M, Trabulsi LR, Keller R, Frankel G, Sperandio V.
Lack
of expression of bundle-forming pili in some clinical isolates
of enteropathogenic Escherichia coli (EPEC) is due to a
conserved large deletion in the bfp operon. FEMS Microbiol
Lett 1999;179:169-74.
- Pelayo JS, Scaletsky IC, Pedroso MZ, Sperandio V, Giron JA,
Frankel G, et al. Virulence
properties of atypical EPEC strains. J Med Microbiol 1999;48:41-9.
- Whittam TS, McGraw EA. Clonal analysis of EPEC
serogroups. Rev Microbiol 1996;27:7-16.
- Fernandes RM, Ramos SR, Rassi V, Blake PA, Gomes TAT. Use of
plasmid profiles to differentiate strains within specific serotypes
of classical enteropathogenic Escherichia coli. Braz J
Med Bio Res 1992;25:667-72.
- Levine MM, Bergquist EJ, Nalin DR, Waterman DH, Hornick RB,
Young CR, et al. Escherichia
coli
strains that cause diarrhoea but do not produce heat-labile or
heat-stable enterotoxins and are non-invasive. Lancet 1978;1:1119-22.
- Smith H, Scotland S, Cheasty T, Willshaw G, Rowe B. Enteropathogenic
Escherichia coli infections in the United Kingdom.
Rev Microbiol, São Paulo 1996;27:45-9.
- Levine MM, Nataro JP, Karch H, Baldini MM, Kaper JB, Black RE,
et al. The diarrheal response of humans to some classic serotypes
of enteropathogenic Escherichia coli is dependent on a
plasmid encoding an enteroadhesiveness factor. J Infect Dis 1985;152:550-9.
- Toledo MRF, Alvariza MCB, Murahovschi J, Ramos SRTS, Trabulsi
LR. Enteropathogenic
Escherichia coli serotypes and endemic diarrhea in infants.
Infect Immun 1983;39:586-9.
- Gomes TAT, Rassi V, MacDonald KL, Ramos SR, Trabulsi LR, Vieira
MA, et al.
Enteropathogens associated with acute diarrheal disease in urban
infants in Sao Paulo, Brazil. J Infect Dis 1991;164:331-7.
- Martinez MB, Taddei CR, Ruiz-Tagle A, Trabulsi LR, Giron JA.
Antibody
response of children with enteropathogenic Escherichia coli
infection to the bundle-forming pilus and locus of enterocyte
effacement-encoded virulence determinants. J Infect Dis 1999;179:269-74.
- Parissi-Crivelli A, Parissi-Crivelli J, Girón J. Recognition
of enteropathogenic Escherichia coli virulence determinants
by human colostrum and serum antibodies. J Clin Microbiol
2000;38:2696-700.
- Loureiro I, Frankel G, Adu-Bobie J, Dougan G, Trabulsi LR, Carneiro-Sampaio
MM. Human
colostrum contains IgA antibodies reactive to enteropathogenic
Escherichia coli virulence-associated proteins:intimin,
BfpA, EspA, and EspB. J Pediatr Gastroenterol Nutr 1998;27:166-71.
- Viljanen M, Peltola T, Junnila S, Olkkonen
L, Järvinen H, Kuistila M, et al. Outbreak
of diarrhoea due Escherichia coli O111:B4 in schoolchildren
and adults: association of Vi antigen-like reactivity. Lancet
1990;336:831-4.
- Kauffmann F, Orskov F. Die Bakteriologie der Escherichia
coli-Enteritis. In: Adam A, editor. Säuglings-Enteritis. Stuttgart:
Georg Thieme Verlag; 1956. p.1-41.
- Bokete TN, Whittam TS, Wilson RA, Clausen CR, O'Callahan CM,
Mosely SL, et al. Genetic
and phenotypic analysis of Escherichia coli with enteropathogenic
characteristics isolated from Seattle children. J Infect Dis
1997;175:1382-9.
- Gomes TAT, Vieira MA, Wachsmuth IK, Blake PA, Trabulsi LR.
Serotype-specific prevalence of Escherichia coli strains
with EPEC adherence factor genes in infants with and without diarrhea
in São Paulo, Brazil. J Infect Dis 1989;160:131-5.
- Griffin P. Epidemiology of Shiga toxin-producing Escherichia
coli infections in humans in the United States. In: Kaper
JB, editor. Escherichia coli O157:H7 and other Shiga toxin-producing
E. coli strains. Washington: American Society of Microbiology;
1998. p. 15-22.
- Gyles C. Escherichia coli in domestic animals. Wallinggford,
UK: CAB International; 1994.
- Saridakis H. Non production of Shiga-like toxins by Escherichia
coli serogroup O26. Rev Microbiol, São Paulo 1994;25:154-5.
- Ewing W, Davis D, Montague T. Studies on the occurrence of Escherichia
coli serotypes associated with diarrheal disease. Atlanta:
US Department of Health, Education and Welfare, Public Health
Service, Communicable Disease Center; 1963.
- Trabulsi L, Campos L, Whittam T, Gomes T, Rodrigues J, Gonçalves
A. Traditional and non-traditional enteropathogenic Escherichia
coli serogroups. Rev Microbiol, São Paulo 1996;27:1-6.
- Vieira M, Andrade J, Trabulsi L, Rosa A, Dias A, Ramos S, et
al. Phenotypic
and genotypic characteristics of Escherichia coli strains
of non-enteropathogenic E. coli (EPEC) serogroups that
carry eae and lack the EPEC adherence factor and Shiga
toxin DNA probe sequences. J Infect Dis 2001;183:762-72.
- Hedberg C, Savarino S, Besser J, Paulus C, Thelen V, Myers L,
et al. An
outbreak of foodborne illness caused by Escherichia coli
O39:NM, an agent not fitting into the existing scheme for classifying
diarrheogenic E. coli. J Infect Dis 1997;176:1625-8.
Table
1. Frequently isolated enteropathogenic Escherichia coli(EPEC)
serotypes, including typical and atypical strains |
|
Strains |
Serotypes |
|
Typical |
O55:[H6], O86:H34, O111:[H2],a
O114:H2, O119:[H6], O127:H6, O142:H6, O142:H34
|
|
|
Atypical
|
O26:H[11], O55:[H7], O55:H34, O86:H8, O111ac:[H8],
O111:[H9], O111:H25, O119:H2, O125ac:H6, O128:H2
|
|
aBrackets denote the frequent occurrence
of nonmotile strains.
|
Table
2. Virulence characteristics not encoded on the locus of
enterocyte effacement (LEE) of atypical enteropathogenic Escherichia
coli (EPEC) strains isolated in São Paulo,
Brazil |
|
Serotype |
Characteristics
|
|
O26:[H11]a
|
EAST1, E-hlyb
|
O55:[H7]
|
EAST1, Afa
|
O111ac:[H8]
|
E-hly
|
O111:[H9]
|
E-hly
|
O119:H2
|
EAST1
|
O125ac:H6
|
AA
|
O128:H2
|
EAST1
|
|
aBrackets denote the frequent occurrence
of nonmotile strains.
bEAST, heat-stable toxin 1 of EAEC; E-hly, EHEC
hemolysin; AA, aggregative adherence; Afa, afimbrial adhesin.
|
Table
3. Intimin types of typical and atypical enteropathogenic
Escherichia coli (EPEC) serotypes |
|
Intimin types
|
Typical
|
Atypical
|
|
Alpha
|
O55:[H6],a O127:H6, O142:H6, O142:H34
|
O111:[H9], O125ac:H6
|
Beta
|
O111:[H2], O114:H2, O119:[H6]
|
O26:H[11], O119:H2, O128:H2
|
Gamma
|
|
O55:[H7], O111ac:[H8]
|
Delta
|
O86:H34
|
|
|
|
|